Abundance, habitat use and diet of Callicebus nigrifrons Spix (Primates, Pitheciidae) in Cantareira State Park, São Paulo, Brazil

Leonardo C. Trevelin 1; Marcio Port-Carvalho 2; Maurício Silveira 3 & Eduardo Morell 4

1 Departamento de Zoologia, Universidade Estadual Paulista. Avenida 24 A 1515, 13506-900 Rio Claro, São Paulo, Brasil. E-mail: [email protected] 2 Seção de Animais Silvestres, Instituto Florestal. Rua do Horto 931, 02377-000 São Paulo, São Paulo, Brasil. E-mail: [email protected] 3 Rua 1, 2124, Centro, 13506-000 Rio Claro, São Paulo, Brasil. E-mail: [email protected] 4 Rua José dos Santos Castro 92, 02375-010 São Paulo, São Paulo, Brasil. E-mail: [email protected]

ABSTRACT. Between april 2005 and May 2006, according to the pressuposts of line transect methodology, census were carried to estimate abundance and population density of Callicebus nigrifrons Spix, 1823 (Pitheciidae) in Cantareira State Park, State of São Paulo, southeastern Brazil (23°23’42”S, 46°35’27”W). After 275.80 Km of census sampling effort, the titis were the second most abundant primate species, presenting an abundance index of 1.4 groups for each 10 km walked and a density estimate of 12.21 ind./km2 (ranging between 8.45 a 17.63 ind./ km2). The collection of ancillary data during the census allowed the determination of diet and habitat use by the titis groups, and results show a relative adaptability to disturbed habitats. KEYWORDS. Atlantic forest; black-fronted titi monkey; conservation; density.

RESUMO. Abundânciaundância, uso do habitat e dieta de Callicebus nigrifrons É. Geoffroy (Primatesimates, Pitheciidae) no Parque Estadual da Cantareiraa, São PauloPaulo, Brasil. Entre abril de 2005 e maio de 2006, através de censos seguindo os pressupostos da metodologia de transecção linear, foram estimadas a densidade populacional e abundância de Callicebus nigrifrons Spix, 1823 (Pitheciidae) no Parque Estadual da Cantareira, Estado de São Paulo, Sudeste do Brasil (23°23’42”S, 46°35’27”W). Com um esforço amostral de 275,8 km de censos, os sauás foram a segunda espécie de primata mais abundante, apresentando um índice de abundância de 1,4 grupos para cada 10 km percorridos e uma estimativa de densidade de 12,21 ind./km2 (variando de 8,45 a 17,63 ind./km2). A coleta de dados auxiliares durante os censos possibilitou a verificação da dieta e uso do hábitat pelos grupos de Callicebus, e os resultados evidenciaram uma relativa adaptabilidade à ambientes perturbados. PALAVRAS-CHAVE. Conservação; densidade; sauás; Mata atlântica.

Titi monkeys, genus Callicebus (Thomas, 1903), are a di- this situation, C. nigrifrons has been assigned to the near threat- verse group of neotropical primates found in the Amazon and ened IUCN category (RYLANDS et al. 2003). Orinoco basins, the Brazilian Atlantic Forest, and the Chaco While there is a growing body on knowledge on the ecol- forests of Paraguay and Bolivia (VAN ROOSMALEN et al. 2002, ogy and conservation of most Atlantic Forest primate genera, NORCONK 2007). Callicebus nigrifrons (Spix, 1823) (Pitheciidae) little is known of most Callicebus species, which include the re- occurs in the Brazilian states of Rio de Janeiro, São Paulo, and cently discovered Callicebus coimbrai (Kobayashi & Langguth, Minas Gerais. It occurs on both banks of the upper São Fran- 1999) (Pitheciidae) (KOBAYASHI & LANGGUTH 1999). Available stud- cisco river, ranging eastwards as far as the distribution of ies have focused on Callicebus personatus (PRICE & PIEDADE 2001a, Callicebus personatus (É. Geoffroy, 1812) (Pitheciidae) (VAN b) and Callicebus melanochir (Wied-Neuwied, 1820) (Pitheciidae) ROOSMALEN et al. 2002). (MÜLLER 1996), although some data are available on populations This range coincides with the most densely populated of C. nigrifrons (OLIVEIRA et al. 2003, SÃO BERNARDO & GALETTI 2004). part of Brazil, which has a long history of colonization and This study presents the results of a survey of the C. nigrifrons deforestation (DEAN 1995). Present-day populations of C. population of the Cantareira State Park in São Paulo, which in- nigrifrons are restricted to forest patches within a highly frag- cludes detailed information on habitat use and diet. The park is mented landscape, where local extinction is a constant threat a relatively large remnant of the original Atlantic Forest, located (VAN ROOSMALEN et al. 2002, SÃO BERNARDO & GALETTI 2004). Given entirely within São Paulo, the largest city in South America.

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MATERIAL AND METHODS different habitat types (corrected by sampling effort), and tested by chi-square (␹2), following the studies of PERES (1993), BOBADILLA Study area & FERRARI (2000), and PORT-CARVALHO & FERRARI (2004). Situated in the Serra da Cantareira (23°23’42”S, 46°35’ Analysis of the use of vertical space was based on 5-m 27”W), between the municipalities of São Paulo, Caieiras, Mairi- height classes, following PERES (1993) and BOBADILLA & FERRARI porã and Guarulhos, the Cantareira State Park (CSP) is a 7,917 (2000). Survey data on the diet of C. nigrifrons were comple- ha protected area administrated by the São Paulo state Forestry mented by ad libitum observations throughout the study pe- Institute. Totally encompassed by the urban area of São Paulo, riod. Specimens were obtained from plants exploited by the Cantareira is not only the World’s largest urban forest, but is titis for identification by a specialist. also one of the most important remnants of the state’s Atlantic Forest, and thus has a considerable potential for the conserva- RESULTS tion of local biodiversity. The park is divided into four admin- Abundance istrative nuclei (Fig. 1), three of which (Pedra Grande, Águas During the 13 month period, we walked a 98.4 km on Claras, and Engordador) were surveyed during the present study. the Águas Claras Nucleus, 98.6 km on the Pedra Grande Surveys Nucleus and 78.8 km on the Engordador Nucleus, with a to- To estimate relative abundance, and population density tal of 275.8 km sample effort, divided in 237 census sessions. and size, primates were surveyed in Cantareira State Park using The number of sessions in each trail varied from 15 to 25, so standard line transect methodology (BURNHAM et al. 1980, BUCK- that the total sample effort in each trail was approximately LAND et al. 1993), between April 2005 and May 2006. Transects the same for that nucleus. A total of 203 primate sightings were conducted along 12 trails, four trails located in each one were obtained, from witch 39 belonged to groups of Callicebus of the nuclei. Transects length varied from 0.8 km to 6 Km, nigrifrons, approximately 19% of all sightings. On the other with a total length of 19.05 km. During surveys, special atten- 164 sightings, we encountered the following primate species tion was paid to the collection of complementary data on the (in order of encounters): Alouatta clamitans (Cabrera, 1940) diet and use of habitat (habitat type and vertical spacing) by C. (Atelidae), Cebus nigritus (Goldfuss, 1809) (Cebidae) and nigrifrons. Callithrix aurita (É. Geoffroy, 1812) (Callitrichidae). Callicebus Habitat was classified according to the schemes provided nigrifrons was the second most abundant species, presenting by previous studies at the site (BAITELLO et al. 1993), modified an abundance index of 1.4 groups for each 10 km walked. according to the aims of the present study, with an emphasis Table II presents this global abundance index as well as the on species composition and sucessional stage (Tab. I). The domi- same index for each nucleus. nant habitat observed along each 50-m interval of the transects The average size of troops found in this study was 2.27 was assigned to one of these categories, providing an estimate individuals per sighting (range = one to five individuals), a of the relative cover of each forest type. Habitat preferences slightly smaller troop size than usually observed for this genus were assessed by comparing observed visitation rates (sightings) (PINTO et al. 1993, NORCONK 2007). Sample size was not large with those expected according to the relative availability of enough for reliable calculations of the Effective Strip Width

Table I. Habitat categories used in the present study. Forest category Description Primary Continuous canopy with tall trees (> 20 m in height) and emergents, low density of lianas, and three well-defined strata Late secondary Discontinuous canopy (15-20 m tall) with few emergents, medium density of lianas, and two strata Early secondary Discontinuous canopy (< 15 m tall), very high density of lianas, and single stratum with dense vegetation Exotic Dominated by Eucalyptus spp., Pinus spp. and Cryptomeria spp. plantations, with sparse understorey of native species Araucaria Dominated by Araucaria angustifolia, with dense understorey of native species

Table II. Survey sightings (per 10 km walked) of the primate species observed in the Cantareira State Park. Nucleus Callicebus nigrifrons Alouatta clamitans Callithrix aurita Cebus nigritus All primates Águas Claras 17 (1.73) 38 (3.86) 6 (0.61) 11 (1.12) 72 (7.32) Pedra Grande 10 (1.01) 80 (8.11) 3 (0.30) 3 (0.30) 96 (9.74) Engordador 12 (1.52) 17 (2.16) 5 (0.60) 1 (0.13) 35 (4.44) All sites 39 (1.41) 135 (4.90) 14 (0.51) 15 (0.54) 203 (7.36)

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Figure 1. Localization of the Cantareira State Park in the Brazilian state of São Paulo and trails used in the study.

(ESW) and the density parameter in each nucleus separately. Habitat use Thus the sighting data were pooled and analyzed for the area To obtain a reliable statistical analysis, the frequency of as a whole. The perpendicular sighting distances were tested each available habitat, as well as the titi’s sightings obtained for normality (Kolmogorov-Smirnov: 0.1321, p > 0.05) and later on each nucleus were grouped and analyzed, statistically, in a analyzed with the parametric ANOVA one-way test (F: 0.9085; global way. Since the trails used during the census where of p = 0.5852). It was possible therefore to generate overall den- different length and were walked distinctively, the total habi- sity estimation based on the pooled data for the area as a whole tat availability was calculated in function of the effort employed (CHIARELLO & MELO 2001), since there was no significant differ- on each trail (Tab. IV). ence between the three nuclei. The uniform key function with In the habitat preference analyses, some patterns could be the cosine expansion was chosen, witch provided the best fit verified, although no significant preference was confirmed for (AIC = 184.10; GOF: P = 0.84071), although other models pro- any special habitat (␹2 = 4.546, df = 4, p > 0.05). The Exotic For- vided similar estimates of density, witch may be interpreted as est and the Initial Secondary Forest habitats didn’t obtain any data consistency (Tab. III). titi records and the Late Secondary Forest habitat obtained an

Table III. Estimated parameters using program Distance Sampling 4.1 (BUCKLAND et al. 1993). Density ESW Abundance in sampled area (individuals) Population size (individuals) a (km2) CV (%) (m) CV (%) 12,21 18.84 14.78 7.04 475 967 (8.45-17,63) (12.81-17.05) (329-685) (670-1395) a Estimated values obtained trough extrapolation for the whole CSP area (7916.52 ha) from the abundance data in the sampled area (3887 ha).

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Table IV. Proportion of habitats sampled (%), sample effort (km) and nucleus representativity (%). Habitats sampled (%) Localities Exotic Araucária Initial Secondary Late Secondary Primary Effort (km) Representativity (%) Forest Forest Forest Forest Forest Águas Claras 6.28 61.94 0.43 25.41 5.95 98.4 35.68 Pedra Grande 0.00 0.00 6.34 77.99 15.67 98.6 35.75 Engordador 0.00 0.00 1.90 54.70 43.40 78.8 28.57 Total 2.24 22.10 2.96 52.57 20.12 275.8 100.00

inferior number than expected, while the Araucaria Forest and most the species (Tab. V). We also observed some individuals the “Primary” Forest obtained more records than it was expected. ingesting arthropods on three occasions, indicating this food The height data on witch the titis were sighted were also item may complete the titis diet. pooled and analyzed as a whole, in order to make the analyses more robust. Also, with the same objective, and only for this DISCUSSION analyses, the data obtained in opportunistic encounters (ad li- The density and relative abundance estimates of the bitum) during the study where also considered, raising the num- present study conform to similar studies carried out with spe- ber of records from 39 to 60 (Fig. 2). cies of the Callicebus genus in Brazilian Atlantic Forest (Tab. VI). Overall, there was a predominance of sightings in the for- Abundance indexes expressed little difference between nu- est canopy, the “10 to 14 m” class or lower canopy, the “15 to 19 clei, except for the smaller Pedra Grande, were the total primate m” class or intermediate canopy, and from “20 to 24 m” class or abundance was greater. This difference was probably related to superior canopy, that together were responsible for 77% of the the very high abundance of howler monkeys Alouatta clamitans, Callicebus sightings. We also noticed that the titis came down to in contrast with the reduction of abundance indexes for the sub-canopy layer frequently (20% of the records), “05 to 09 Calllithrix aurita, Cebus nigritus and the titis. The Pedra Grande m” class, and also occasionally used the emergent trees over the nucleus had the greatest secondary forest availability, and the forest canopy, “25 to 30 m” class, with 3% of the records. tourist pressure is often more intense, compared with the other Diet nuclei. Despite this difference, the titis were the second most We observed the titis consume 15 species belonging to abundant primate species in all nuclei in CSP, and presented an nine families. Fruit pulp was the principal item consumed for overall density estimate larger than most of the studies presented

Table V. Plant species consumed by Callicebus nigrifrons during the study. Family Species Habitus Item consumed Bignoniaceae Pithecoctenium sp. Tree Imature seed * Euphorbiaceae Alchornea triplinervia Tree Fruit Tetrorchidium rubrivenium Tree Fruit Croton floribundus Tree Seed Fabaceae Inga sessilis Tree Fruit and flower Inga marginata Tree Fruit Lauraceae Persea americana Tree Fruit Melastomataceae Miconia cinnamomifolia Tree Leaf Myrtaceae Eugenia involucrata Tree Fruit Myrciaria sp. Tree Fruit Psidium guajava Tree Fruit Rosaceae Prunnus sellowiana Tree Leaf Sapindaceae Cupania oblongifolia Tree Fruit Paullinia sp. Liana Fruit Solanaceae Solanum mauritianum Tree Fruit, flower, imature leaf and branch * The collected material contained a Coleopteran larva, making it impossible to define precisely the consumed item.

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Figure 2. Ideal vegetation profile in Cantareira State Park with the vertical layer usage frequency by Callicebus nigrifrons.

in table VI, although they had a slightly lower troop size (2.27 2002, SÃO BERNARDO & GALETTI 2004, MARTINS 2005). However, HEIDUCK individuals) than observed in most studies (PINTO et al. 1993, (2002) showed that despite utilizing both secondary and primary NORCONK 2007). Some of this variation can be explained by sample forests, the home ranges of troops always contained a major por- differences and systematic errors that may arrise whith viola- tion of primary forest, and that habitat use was much more re- tions of the basic assumptions of line transect census theory, lated to food resource availability than the proportional avail- but can we hypothesize this as adaptations to perturbation? ability of each habitat. In the CSP, C. nigrifrons did not show any CHIARELLO (2003), comparing primate census data for São Paulo statistically significant preference for any kind of habitat, occur- and Espírito Santo, could not find any correlation between frag- ring in all habitats, except for initial secondary and exotic forests. ment size and density/abundance parameters for most primates, With regard to the vertical stratification observed, the except for Brachyteles hypoxanthus (Kuhl, 1820) (Atelidae), indi- titis exhibited a considerable preference for the lower canopy cating a certain ecological flexibility of the Brazilian Atlantic (10 to 14 meters class). This corroborates with the overall pat- Forest primates, witch demonstrates a rather extensive adaptative tern relating the height of strata used to body size and locomo- capacity to perturbation caused by fragmentation. tion mode for primates (CUNHA et al. 2006). Callicebus is a me- Some studies relate the occurrence and persistence of titis dium sized primate occurring in all strata, but showing a pref- in secondary forests fragments from several sizes of Brazilian Atlan- erence for intermediate strata (RYLANDS et al. 1996, CUNHA et al. tic forests (STALLINGS & ROBINSON 1991, PINTO et al. 1993, HEIDUCK 2006).

Table VI. Density and relative abundance estimates of Callicebus on different localities of Brazilian Atlantic Forest. Fragment Density Sighting rate Species Study area Reference area (km2) (ind/km2) (groups/10 km) C. nigrifrons Cantareira State Park, São Paulo 79.2 11.21 1.43 Present study

Barreiro Rico, São Paulo 32.6 7.0-10.0 – PINTO et al. (1993)

São José, São Paulo 2.3 3.5 0.56 SÃO BERNARDO & GALETTI (2004)

Serra do Brigadeiro, Minas Gerais 132.1 10.3 – COSENZA & MELO (1998)

Viçosa, Minas Gerais 0.8 14.86 1.83 OLIVEIRA et al. (2003)

C. personatus Augusto Ruschi Biological Reserve, Espírito Santo 40.0 5.4 0.54 PINTO et al. (1993)

Linhares Forest Reserve, Espírito Santo 218.0 7.7 1.23 CHIARELLO & MELO (2001)

Linhares Forest Reserve, Espírito Santo 218.0 12.3-12.6 – PRICE et al. (2002)

M7/317, Espírito Santo 2.6 1.4 0.22 CHIARELLO & MELO (2001)

Putiri, Espírito Santo 2.1 6.4 1.02 CHIARELLO & MELO (2001)

Sooretama Biological Reserve, Espírito Santo 242.5 9.5 1.66 CHIARELLO & MELO (2001)

C. melanochir CEPLAC, Bahia 10.0 17.0 – MÜLLER (1996)

Teimoso Farm, Bahia 2.4 17.7 – PINTO et al. (1993)

Una, Bahia 1.0 3.4-16.7 – PINTO et al. (1993)

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Observations of plant species consumed by C. nigrifrons 2000), pointing this as a possible immediate threat to their are consistent with the literature, especially with the basically long-term conservation. frugivorous pattern of diet (NORCONK 2007). However, the actual This and other problems for the conservation not only of components of this diet are subject to debate, since various spe- the titis, but of all other primate species that occur in the CSP cies of the Callicebus personatus group, especially C. nigrifrons are closely related to its proximity to the biggest urban center of show much variation in specific diet. KINZEY & BECKER (1983) Latin America. To guarantee the long term conservation of these studying C. personatus, MÜLLER (1996) studying C. melanochir and primates in the metropolitan region of São Paulo city, legal and PRICE & PIEDADE (2001a) also studying the C. personatus species political measures and concrete actions must be orchestrated in found the complement of diet to consist entirely of leaves, while conformity with a pre-defined strategy that supports the con- HEIDUCK (1997) working with C. melanochir relate a diet comple- servation of this and other taxa (CHIARELLO 2003). mented with insects in addition to leaves, witch matches the This study showed that the Callicebus nigrifrons popula- observation of this feeding behavior in the CSP. Other interest- tion in CSP, a medium sized primate species with intermediate ing aspect was the major presence of typically secondary species abundance in the primate community, is comparatively well in the titis diet, especially the tapiá (Alchornea triplinervia) and established in this 7,917 ha forest reserve. They present almost the ingás (Inga sessilis e I. marginata), which were frequently re- no habitat limitation on occurrence, responding well to second- corded during their fruiting season. Could these records again ary forest, a predominant habitat in the CSP. The population be evidence of the high adaptability of this species to secondary size we estimated could guarantee its short-term survival, but in forest areas? This feeding flexibility and consequent adaptabil- the long-term, roads and the urbanization of the park´s surround- ity to variations in resource availability, in terms of component ings may represent a considerable threat for its conservation. diversity and feeding behavior, could explain not only these re- gional differences in diet but also the apparent persistence suc- ACKNOWLEDGMENTS cess in altered and fragmented forest areas. More specifically To Stephen F. Ferrari and two anonymous reviewers for designed studies of diet aiming to solve these ecological ques- the review and valuable comments, to Philipp Withers and tions for titis are of fundamental importance not only to the Cristine Cooper for the help with the English version, to all better understanding of this species, but also to its adequate the personnel in CSP and Forestry Institute of São Paulo for management in protected areas. permitting the realization of this work (SMA Process 42.052/ The population size estimated for CSP by this study was 2005), to the Botanist Geraldo Daher Côrrea Franco (Forestry approximately 967 individuals (Tab. III). If we choose to con- Institute of São Paulo) for the identifications of the botanical sider the average group size of 2.2 individuals obtained by linear specimens, Tessio Novack (INPE) and Cristiano Figueira (FFLCH- transects to be lower than the literature data (NORCONK 2007), USP) for helping with the nuclei areas and the localization map. this estimate may be thought as an underestimate of the true situation. Even so, values somewhat higher than 967 individuals REFERENCES are still smaller than the minimal viable population size of 7,000 individuals, as suggested by REED et al. (2003) to avoid long-term BAITELLO, J.B.; O.T. AGUIAR; F.T. ROCHA; J.A PASTORE & R. ESTEVES. genetics, demographics and stochastic effects. On the other hand, 1993. Estrutura fitossociológica da vegetação arbórea da Serra BRITO & GRELLE (2006) working with stochastic population mod- da Cantareira (SP) – Núcleo Pinheirinho. 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Received in 29.V.2007; accepted in 22.XI.2007.

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